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Title: The Arabidopsis sickle mutant exhibits altered circadian clock responses to cool tempatures and tempature-dependent alternative splicing

Author
item MARSHALL, CARINE - University Of California
item TARTAGLIO, VIRGINIA - University Of California
item DUARTE, MARITZA - University Of California
item Harmon, Frank

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/8/2016
Publication Date: 10/12/2016
Citation: Marshall, C., Tartaglio, V., Duarte, M., Harmon, F.G. 2016. The Arabidopsis sickle mutant exhibits altered circadian clock responses to cool tempatures and tempature-dependent alternative splicing. The Plant Cell. 28(10):2560-2575. doi:10.1105/tpc.16.00223.

Interpretive Summary: The SICKLE gene is necessary for plants to respond correctly to cool temperatures. Global climate change will require crop and wild plants to resist more extreme weather conditions, including low and high temperatures. Plants continuously adapt to environmental conditions by actively sensing and responding to environmental signals through regulatory systems that are incompletely understood. A major contributor to the environmental responses of plants is the circadian clock, which is a self-sustaining molecular timer. In this role, the clock synchronizes environmentally sensitive internal processes with external daily and seasonal environmental conditions. This study describes the sickle mutant discovered in the model plant Arabidopsis thaliana. Plants with the sickle mutation no longer perform normal activities in cool temperature conditions (16-22 degrees C), which impairs the circadian clock. This paper shows the SICKLE gene participates in the fundamental regulatory system known as alternative splicing of transcripts. Alternative splicing is a newly recognized way that plants use to resist environmental stresses. Because SICKLE is a gene present in all flowering plants, including major crop species, the knowledge gained from this study can be potentially translated to both row and specialty crop plants. The recognition that plant stress responses depend on SICKLE-type genes and, alternative splicing in general, means that these genes are potential targets in the effort to increasing crop and biomass production in a changing global climate.

Technical Abstract: The circadian clock allows plants to anticipate and respond to daily changes in ambient temperature. Mechanisms establishing the timing of circadian rhythms in Arabidopsis thaliana through temperature entrainment remain unclear. Also incompletely understood is the temperature compensation mechanism that maintains consistent period length within a range of ambient temperatures. A genetic screen for Arabidopsis mutants affecting temperature regulation of the PSEUDO-RESPONSE REGULATOR7 promoter yielded a novel allele of the SICKLE (SIC) gene. This mutant, sic-3, and the existing sic- 1 mutant both exhibit low-amplitude or arrhythmic expression of core circadian clock genes under cool ambient temperature cycles, but not under light-dark entrainment. sic mutants also lengthen free running period in a manner consistent with impaired temperature compensation. sic mutant alleles accumulate LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED1 (CCA1) splice variants, among other alternatively spliced transcripts, which is exacerbated by cool temperatures. The cca1-1 lhy-20 double mutant is epistatic to sic-3, indicating the LHY and CCA1 splice variants are needed for sic-3 circadian clock phenotypes. It is not expected that SIC is directly involved in the circadian clock mechanism; instead, SIC likely contributes to pre-mRNA metabolism, and the splice variants that accumulate in sic mutants likely affect the circadian clock response to cool ambient temperature.